Abstract
Cells of the early Caenorhabditis elegans embryo divide in an invariant pattern. Here I show that the division axes of some early cells (EMS and E) are controlled by specific cell-cell contacts (EMS-P2 or E-P3 contact). Altering the orientation of contact between these cells alters the axis along which the mitotic spindle is established, and hence the orientation of cell division. Contact-dependent mitotic spindle orientation appears to work by establishing a site of the type described by Hyman and White (1987. J. Cell Biol. 105:2123-2135) in the cortex of the responding cell: one centrosome moves toward the site of cell-cell contact during centrosome rotation in both intact embryos and reoriented cell pairs. The effect is especially apparent when two donor cells are placed on one side of the responding cell: both centrosomes are "captured," pulling the nucleus to one side of the cell. No centrosome rotation occurs in the absence of cell-cell contact, nor in nocodazole-treated cell pairs. The results suggest that some of the cortical sites described by Hyman and White are established cell autonomously (in P1, P2, and P3), and some are established by cell-cell contact (in EMS and E). Additional evidence presented here suggests that in the EMS cell, contact-dependent spindle orientation ensures a cleavage plane that will partition developmental information, received by induction, to one of EMS's daughter cells.
Full Text
The Full Text of this article is available as a PDF (2.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Albertson D. G. Formation of the first cleavage spindle in nematode embryos. Dev Biol. 1984 Jan;101(1):61–72. doi: 10.1016/0012-1606(84)90117-9. [DOI] [PubMed] [Google Scholar]
- Chant J. Cell polarity in yeast. Trends Genet. 1994 Sep;10(9):328–333. doi: 10.1016/0168-9525(94)90036-1. [DOI] [PubMed] [Google Scholar]
- Chenevert J. Cell polarization directed by extracellular cues in yeast. Mol Biol Cell. 1994 Nov;5(11):1169–1175. doi: 10.1091/mbc.5.11.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eshel D., Urrestarazu L. A., Vissers S., Jauniaux J. C., van Vliet-Reedijk J. C., Planta R. J., Gibbons I. R. Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11172–11176. doi: 10.1073/pnas.90.23.11172. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldstein B. An analysis of the response to gut induction in the C. elegans embryo. Development. 1995 Apr;121(4):1227–1236. doi: 10.1242/dev.121.4.1227. [DOI] [PubMed] [Google Scholar]
- Goldstein B. Establishment of gut fate in the E lineage of C. elegans: the roles of lineage-dependent mechanisms and cell interactions. Development. 1993 Aug;118(4):1267–1277. doi: 10.1242/dev.118.4.1267. [DOI] [PubMed] [Google Scholar]
- Goldstein B., Hird S. N., White J. G. Cell polarity in early C. elegans development. Dev Suppl. 1993:279–287. [PubMed] [Google Scholar]
- Hill R. J., Sternberg P. W. Cell fate patterning during C. elegans vulval development. Dev Suppl. 1993:9–18. [PubMed] [Google Scholar]
- Hird S. N., White J. G. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J Cell Biol. 1993 Jun;121(6):1343–1355. doi: 10.1083/jcb.121.6.1343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hyman A. A. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position. J Cell Biol. 1989 Sep;109(3):1185–1193. doi: 10.1083/jcb.109.3.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hyman A. A., White J. G. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J Cell Biol. 1987 Nov;105(5):2123–2135. doi: 10.1083/jcb.105.5.2123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kilmartin J. V., Wright B., Milstein C. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J Cell Biol. 1982 Jun;93(3):576–582. doi: 10.1083/jcb.93.3.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li Y. Y., Yeh E., Hays T., Bloom K. Disruption of mitotic spindle orientation in a yeast dynein mutant. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10096–10100. doi: 10.1073/pnas.90.21.10096. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lutz D. A., Hamaguchi Y., Inoué S. Micromanipulation studies of the asymmetric positioning of the maturation spindle in Chaetopterus sp. oocytes: I. Anchorage of the spindle to the cortex and migration of a displaced spindle. Cell Motil Cytoskeleton. 1988;11(2):83–96. doi: 10.1002/cm.970110202. [DOI] [PubMed] [Google Scholar]
- Muhua L., Karpova T. S., Cooper J. A. A yeast actin-related protein homologous to that in vertebrate dynactin complex is important for spindle orientation and nuclear migration. Cell. 1994 Aug 26;78(4):669–679. doi: 10.1016/0092-8674(94)90531-2. [DOI] [PubMed] [Google Scholar]
- Palmer R. E., Sullivan D. S., Huffaker T., Koshland D. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J Cell Biol. 1992 Nov;119(3):583–593. doi: 10.1083/jcb.119.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- RAPPAPORT R. Experiments concerning the cleavage stimulus in sand dollar eggs. J Exp Zool. 1961 Oct;148:81–89. doi: 10.1002/jez.1401480107. [DOI] [PubMed] [Google Scholar]
- Schierenberg E. Reversal of cellular polarity and early cell-cell interaction in the embryos of Caenorhabditis elegans. Dev Biol. 1987 Aug;122(2):452–463. doi: 10.1016/0012-1606(87)90309-5. [DOI] [PubMed] [Google Scholar]
- Siddiqui S. S., Babu P. Genetic mosaics of Caenorhabditis elegans: a tissue-specific fluorescent mutant. Science. 1980 Oct 17;210(4467):330–332. doi: 10.1126/science.7423194. [DOI] [PubMed] [Google Scholar]
- Strome S. Determination of cleavage planes. Cell. 1993 Jan 15;72(1):3–6. doi: 10.1016/0092-8674(93)90041-n. [DOI] [PubMed] [Google Scholar]
- Strome S., Wood W. B. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell. 1983 Nov;35(1):15–25. doi: 10.1016/0092-8674(83)90203-9. [DOI] [PubMed] [Google Scholar]
- Strome S., Wood W. B. Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1558–1562. doi: 10.1073/pnas.79.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sullivan D. S., Huffaker T. C. Astral microtubules are not required for anaphase B in Saccharomyces cerevisiae. J Cell Biol. 1992 Oct;119(2):379–388. doi: 10.1083/jcb.119.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sulston J. E., Schierenberg E., White J. G., Thomson J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983 Nov;100(1):64–119. doi: 10.1016/0012-1606(83)90201-4. [DOI] [PubMed] [Google Scholar]
- Symes K., Weisblat D. A. An investigation of the specification of unequal cleavages in leech embryos. Dev Biol. 1992 Mar;150(1):203–218. doi: 10.1016/0012-1606(92)90019-d. [DOI] [PubMed] [Google Scholar]
- Waddle J. A., Cooper J. A., Waterston R. H. The alpha and beta subunits of nematode actin capping protein function in yeast. Mol Biol Cell. 1993 Sep;4(9):907–917. doi: 10.1091/mbc.4.9.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waddle J. A., Cooper J. A., Waterston R. H. Transient localized accumulation of actin in Caenorhabditis elegans blastomeres with oriented asymmetric divisions. Development. 1994 Aug;120(8):2317–2328. doi: 10.1242/dev.120.8.2317. [DOI] [PubMed] [Google Scholar]
- Whittaker J. R. Acetylcholinesterase development in extra cells caused by changing the distribution of myoplasm in ascidian embryos. J Embryol Exp Morphol. 1980 Feb;55:343–354. [PubMed] [Google Scholar]